One cell swallows another and puts it to work; then it gets swallowed up. In the early history of life, this happened a lot.
Chimeras--creatures produced from a mingling of diverse organisms--have long been the stuff of legend. But they are in fact an ancient and ubiquitous form of life. About 600 million years ago, one cell swallowed another--a bacterium that had the ability to harness the energy of sunlight--and instead of digesting it, put it to work. Eons later the progeny of that distant enslavement are ensconced in the cells of every plant: they are the light-trapping organelles known as chloroplasts. A similar engulfment produced the mitochondria, the tiny power plants that are present in plant and animal cells alike--indeed in all eukaryotes, as cells with a nucleus are called. We are all of us chimeras now.
This theory of endosymbiosis (meaning living together within) was radical when it was first proposed almost a century ago, but it is nearly gospel among biologists today. (Some of them even think cell nuclei are former bacteria.) What is more recent is the realization that endosymbiotic engulfment was not always a onetime thing--not a case of eukaryote eats bacterium, acquires chloroplast, end of story. Instead it seems the story goes on and turns cannibalistic: the eukaryote is itself eaten by another eukaryote, which steals the chloroplast and is then perhaps engulfed in its turn. This type of double and even triple engulfment apparently occurred so often in the early history of life on Earth that some researchers believe it played a crucial role in evolution. For instance, it may be responsible for the tremendous diversity of algae in rivers and oceans today.
The latest evidence comes from plant cell biologist Geoffrey McFadden and his colleagues at the University of Melbourne in Australia and the University of Freiburg in Germany. They have been studying some oddball organisms called chlorarachniophytes. These creatures are animals like amoebas, in that they eat things. But they are also algae, in that they are solar powered: they have a light-catching chloroplast. And that chloroplast, unlike the conventional chloroplast, is surrounded by four membranes instead of two.
That alone is evidence of a double engulfment. Of the four membranes, says McFadden, the two inner ones would have belonged to the original bacterium. (It had a double outer membrane.) The third membrane belonged to the first eukaryote that engulfed the bacterium, and the fourth is what’s left of the food vacuole--the stomach, as it were--with which the chlorarachniophyte engulfed the first eukaryote. This view of how the chlorarachniophyte got its chloroplast is not new to McFadden, but he has found genetic evidence to prove it.
Lodged snugly between the second and third membranes of the choroplast is a structure that is called a nucleomorph because it resembles a cell nucleus. In fact, says McFadden, the nucleomorph is a nucleus, or the remains of one: the nucleus of the swallowed-up eukaryote. It still contains DNA. McFadden and his colleagues extracted this DNA in a mixture with the nuclear DNA of the chlorarachniophyte itself by first grinding up the entire beast. Then they tried to sort out the mix.
They used DNA primers--small stretches of DNA that seek out and bind to their own likeness--to look for a gene that all cells have in some form or another. If all the DNA in the chlorarachniophyte had always belonged to it alone, the researchers would have turned up only one version of the gene. Instead they found two. They tagged the two genes with tiny bits of gold and inserted them back in the cell to see where they had come from. One had come from the chlorarachniophyte’s nucleus. The other had come from the nucleomorph. Apparently it had once belonged to a different cell.
Another bit of evidence came from looking at the chlorarachniophyte’s telomeres. Telomeres are bits of DNA that cap the ends of chromosomes and prevent damage during cell division; their genetic sequence varies radically between kingdoms of organisms. We found that the host cell has telomeres that are more like fungi’s, says McFadden, and the little guy--that is, the chloroplast--has telomeres that are more like plants’. That made sense, since the chloroplast is the source of the organism’s ability to photosynthesize.
McFadden’s genetic work shows that the chlorarachniophytes stole that ability from a eukaryote that had first stolen it from a bacterium. It’s impossible to say when the second theft occurred, but McFadden suspects it happened hundreds of millions of years ago. Presumably an algal cell was engulfed and was somehow able to resist digestion and thrive inside the cell. If the relationship is mutually beneficial, says McFadden, evolutionary pressures will work to stabilize it. Mutually beneficial it clearly is: the chloroplast swaps its cash crop--the sugars it makes in solar-powered reactions--for proteins made in the host cell. Somehow it manages to export and import these molecules across its four membranes.
Over the millennia, in fact, the prey cell has become so dependent on imports from its host that it has shed most of its genes. While the nucleus of the chlorarachniophyte has 16 chromosomes, the nucleomorph has only three--which include just 5 percent, McFadden reckons, of its original complement of genes. The only genes it retains, he explains, are those that are crucial to maintaining the chloroplast. There’s no junk there--just the housekeeping genes needed to replicate the DNA and maintain the structure of the cell. How exactly replication proceeds is something McFadden hasn’t worked out yet. Replication of the host and prey cell has to be timed exactly so, he says, because if the host cell divides before the prey cell, it wouldn’t have the chloroplast it needs to survive.
Chlorarachniophytes are not the only organisms with that problem, because they are far from the only algae that stole their chloroplasts from other eukaryotes. One other type of alga, the cryptomonad, possesses a nucleomorph, and genetic tests have shown that it, too, has DNA that is distinct from the DNA of its host nucleus. In all, aside from the chlorarachniophytes, there are some 27,000 species of alga that have four- membraned chloroplasts. In 1981, University of British Columbia biologist Thomas Cavalier-Smith proposed that these species constitute a separate kingdom of life--the taxonomic equivalent of plants or animals--which he named Chromista. Many biologists have since come to accept his view. Cavalier-Smith believes all the chromist algae acquired their chloroplasts through secondary symbiosis--that is, by absorbing another eukaryote. Over time, though, most of them lost all remnants of a nucleus in the chloroplast.
There is growing evidence that there was a single symbiotic origin of the chloroplast from a primitive bacterium, says Cavalier-Smith. It’s this secondary acquisition of chloroplasts that appears to have happened more than once. If we think carefully, we can explain all the different types of algae by one primary symbiosis involving a bacterium, and between four and six separate instances of secondary symbiosis involving a eukaryote. Cavalier-Smith also knows of at least one instance of what looks like a triple engulfment--a chloroplast-thieving cryptomonad that has been swallowed up by another eukaryote--and he thinks there may have been others. A triple-engulfed chloroplast, he says, would have to lose a couple of membranes in order to function inside its host, and so it would end up looking like a chloroplast that has been swallowed only twice.
To Cavalier-Smith, McFadden’s work on chlorarachniophytes is just the latest evidence that secondary symbiosis has played more than a cameo role in the spectacle of evolution. It was the initial enslavement of a bacterium as a chloroplast that created algae; and a huge new supply of algae may have been the food that helped fuel the explosive diversification of marine animals around 600 million years ago, at the beginning of the Cambrian Period. But it was the secondary symbioses, says Cavalier-Smith, occurring at roughly the same time or somewhat later, that led to the explosive diversification of the algae themselves. More algal species--and algal phyla--arose from a secondary symbiosis than from the primary one, he explains. It probably happened several times, and it has probably contributed more than primary symbiosis to the diversity of algae and plant life.
